Molecular Signatures of Dengue Virus-Specific IL-10/IFN-γ Co-producing CD4 T Cells and Their Association with Dengue Disease
Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL...
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| Published in | Cell reports (Cambridge) Vol. 29; no. 13; pp. 4482 - 4495.e4 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
24.12.2019
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2019.11.098 |
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| Abstract | Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF.
[Display omitted]
•DENV-specific IL-10+IFN-γ+ DP CD4 T cells are prominent during acute disease•Most DP cell DE genes are non-cytotoxic/Tr1 and include IL21, IL22, CD109, and CCR1•DP cells have similar gene expression in DF and DHF, despite higher frequency in DHF•Disease severity is not associated with altered DP cell phenotype or functionality
Tian et al. identify and characterize antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells in acute dengue patients. DP cells display similar transcriptomic profiles in mild DF and severe DHF, despite their increased frequency in DHF, suggesting that DHF is not associated with the altered phenotype or functionality of DP cells. |
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| AbstractList | Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10
IFN-γ
double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF. Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10 + IFN-γ + double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF. Tian et al. identify and characterize antigen-specific IL-10 + IFN-γ + double-positive (DP) CD4 T cells in acute dengue patients. DP cells display similar transcriptomic profiles in mild DF and severe DHF, despite their increased frequency in DHF, suggesting that DHF is not associated with the altered phenotype or functionality of DP cells. Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF. : Tian et al. identify and characterize antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells in acute dengue patients. DP cells display similar transcriptomic profiles in mild DF and severe DHF, despite their increased frequency in DHF, suggesting that DHF is not associated with the altered phenotype or functionality of DP cells. Keywords: dengue virus, dengue fever, dengue hemorrhagic fever, CD4 T cell, IL-10, IFN-γ, RNA-seq, CyTOF, acute dengue, transcriptomics Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF.Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF. Dengue virus (DENV) can cause diseases ranging from dengue fever (DF) to more severe dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Whether antiviral T cells contribute to the protection against or pathogenesis of severe disease is not well defined. Here, we identified antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells during acute DENV infection. While the transcriptomic signatures of DP cells partially overlapped with those of cytotoxic and type 1 regulatory CD4 T cells, the majority of them were non-cytotoxic/Tr1 and included IL21, IL22, CD109, and CCR1. Although we observed a higher frequency of DP cells in DHF, the transcriptomic profile of DP cells was similar in DF and DHF, suggesting that DHF is not associated with the altered phenotypic or functional attributes of DP cells. Overall, this study revealed a DENV-specific DP cell subset in patients with acute dengue disease and argues against altered DP cells as a determinant of DHF. [Display omitted] •DENV-specific IL-10+IFN-γ+ DP CD4 T cells are prominent during acute disease•Most DP cell DE genes are non-cytotoxic/Tr1 and include IL21, IL22, CD109, and CCR1•DP cells have similar gene expression in DF and DHF, despite higher frequency in DHF•Disease severity is not associated with altered DP cell phenotype or functionality Tian et al. identify and characterize antigen-specific IL-10+IFN-γ+ double-positive (DP) CD4 T cells in acute dengue patients. DP cells display similar transcriptomic profiles in mild DF and severe DHF, despite their increased frequency in DHF, suggesting that DHF is not associated with the altered phenotype or functionality of DP cells. |
| Author | Mateus, Jose Vijayanand, Pandurangan De-Oliveira-Pinto, Luzia M. de Silva, Aruna D. Weiskopf, Daniela Peters, Bjoern Wijewickrama, Ananda Sette, Alessandro Seumois, Grégory Tian, Yuan Kim, Cheryl Premawansa, Gayani Grifoni, Alba Harris, Eva Herrera-de la Mata, Sara Goonawardhana, N.D. Suraj Hinz, Denise Balmaseda, Angel Premawansa, Sunil |
| AuthorAffiliation | 3 Department of Paraclinical Sciences, General Sir John Kotelawala Defense University, Ratmalana 10390, Sri Lanka 2 Flow Cytometry Core Facility, La Jolla Institute for Immunology, La Jolla, CA 92037, USA 7 Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministerio de Salud, Managua 16064, Nicaragua 8 Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA 94720, USA 9 Department of Medicine, University of California, San Diego, La Jolla, CA 92093, USA 4 Department of Zoology and Environment Sciences, Faculty of Science, University of Colombo, Colombo 00300, Sri Lanka 6 National Institute of Infectious Diseases, Gothatuwa, Angoda 10620, Sri Lanka 1 Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA 5 North Colombo Teaching Hospital, Ragama 11010, Sri Lanka 10 Lead Contact |
| AuthorAffiliation_xml | – name: 8 Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA 94720, USA – name: 1 Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – name: 3 Department of Paraclinical Sciences, General Sir John Kotelawala Defense University, Ratmalana 10390, Sri Lanka – name: 2 Flow Cytometry Core Facility, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – name: 4 Department of Zoology and Environment Sciences, Faculty of Science, University of Colombo, Colombo 00300, Sri Lanka – name: 5 North Colombo Teaching Hospital, Ragama 11010, Sri Lanka – name: 10 Lead Contact – name: 9 Department of Medicine, University of California, San Diego, La Jolla, CA 92093, USA – name: 7 Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministerio de Salud, Managua 16064, Nicaragua – name: 6 National Institute of Infectious Diseases, Gothatuwa, Angoda 10620, Sri Lanka |
| Author_xml | – sequence: 1 givenname: Yuan surname: Tian fullname: Tian, Yuan email: ytian@lji.org organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 2 givenname: Grégory surname: Seumois fullname: Seumois, Grégory organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 3 givenname: Luzia M. surname: De-Oliveira-Pinto fullname: De-Oliveira-Pinto, Luzia M. organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 4 givenname: Jose surname: Mateus fullname: Mateus, Jose organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 5 givenname: Sara surname: Herrera-de la Mata fullname: Herrera-de la Mata, Sara organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 6 givenname: Cheryl surname: Kim fullname: Kim, Cheryl organization: Flow Cytometry Core Facility, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 7 givenname: Denise surname: Hinz fullname: Hinz, Denise organization: Flow Cytometry Core Facility, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 8 givenname: N.D. Suraj surname: Goonawardhana fullname: Goonawardhana, N.D. Suraj organization: Department of Paraclinical Sciences, General Sir John Kotelawala Defense University, Ratmalana 10390, Sri Lanka – sequence: 9 givenname: Aruna D. surname: de Silva fullname: de Silva, Aruna D. organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 10 givenname: Sunil surname: Premawansa fullname: Premawansa, Sunil organization: Department of Zoology and Environment Sciences, Faculty of Science, University of Colombo, Colombo 00300, Sri Lanka – sequence: 11 givenname: Gayani surname: Premawansa fullname: Premawansa, Gayani organization: North Colombo Teaching Hospital, Ragama 11010, Sri Lanka – sequence: 12 givenname: Ananda surname: Wijewickrama fullname: Wijewickrama, Ananda organization: National Institute of Infectious Diseases, Gothatuwa, Angoda 10620, Sri Lanka – sequence: 13 givenname: Angel surname: Balmaseda fullname: Balmaseda, Angel organization: Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministerio de Salud, Managua 16064, Nicaragua – sequence: 14 givenname: Alba surname: Grifoni fullname: Grifoni, Alba organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 15 givenname: Pandurangan surname: Vijayanand fullname: Vijayanand, Pandurangan organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 16 givenname: Eva surname: Harris fullname: Harris, Eva organization: Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA 94720, USA – sequence: 17 givenname: Bjoern surname: Peters fullname: Peters, Bjoern organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 18 givenname: Alessandro surname: Sette fullname: Sette, Alessandro organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA – sequence: 19 givenname: Daniela surname: Weiskopf fullname: Weiskopf, Daniela organization: Division of Vaccine Discovery, La Jolla Institute for Immunology, La Jolla, CA 92037, USA |
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| Keywords | dengue hemorrhagic fever IFN-γ dengue fever RNA-seq CD4 T cell dengue virus transcriptomics CyTOF IL-10 acute dengue |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Y.T. designed and performed the experiments, analyzed the data, performed computational analysis, and wrote the manuscript. G.S., S.H.-d.l.M., and P.V. prepared the RNA-seq libraries and coordinated RNA-sequencing. L.M.D.-O.-P. and J.M. performed the experiments. C.K. and D.H. helped Y.T. with the CyTOF experiments. N.D.S.G., A.D.d.S., S.P., G.P., A.W., A.B., and E.H. collected samples and provided clinical information. Y.T., A.G., B.P., A.S., and D.W. designed and directed the study and critically edited the manuscript. |
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| Title | Molecular Signatures of Dengue Virus-Specific IL-10/IFN-γ Co-producing CD4 T Cells and Their Association with Dengue Disease |
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